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Antidepressant modulation of isolation and restraint stress effects on brain chemistry and morphology

Published online by Cambridge University Press:  16 April 2020

BS McEwen ,
J Angulo ,
E Gould ,
S Mendelson  and
Y Watanabe
BS McEwen
Affiliation:
Laboratory of Neuroendocrinology, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA
J Angulo
Affiliation:
Laboratory of Neuroendocrinology, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA
E Gould
Affiliation:
Laboratory of Neuroendocrinology, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA
S Mendelson
Affiliation:
Laboratory of Neuroendocrinology, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA
Y Watanabe
Affiliation:
Laboratory of Neuroendocrinology, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA
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Summary

Stress elicits adaptive responses from the brain, but it can also lead to maladaptive consequences. For example, stress can precipitate mental illness, including depression. Prolonged stress also causes damage to neurons in the hippocampus. Antidepressant drugs must be evaluated, not only for their ability to potentiate adaptive responses, but also to inhibit maladaptive consequences of stress. Ongoing research in our laboratory has compared the atypical tricyclic antidepressant, tianeptine, with the typical tricyclics, desipramine and imipramine, with respect to the effects of isolation and repeated restraint stress. Tianeptine and desipramine similarly attenuated isolation stress-induced increases in locus coeruleus and midbrain tyrosine hydroxylase mRNA levels and isolation-stress induced decreases in preproenkephalin mRNA levels in striatum and nucleus accumbens. However, tianeptine and imipramine differed in their effects in the cerebral cortex and hippocampus on 5HT2, and 5HT1A receptor levels but, surprisingly, produced similar effects on levels of the serotonin transporter labelled with [3H] paroxetine. Tianeptine also prevented stress-induced reductions in the length and number of branchpoints of dendrites of CA3 pyramidal neurons in hippocampus; comparison with effects of typical tricyclics are ongoing. Tianeptine also blocked effects of corticosterone treatment to reduce branching and length of CA3 dendrites. These actions of tianeptine may be due to interactions between 5HT and excitatory amino acids in the mossy fiber terminals on CA3 pyramidal neurons. Taken together, these results indicate that tianeptine has unique properties compared to some other antidepressant drugs, but shares in common with those drugs the ability to attenuate stress effects on tyrosine hydroxylase gene expression and on the serotonin transporter. It remains to be seen whether these actions are the basis of a common antidepressant action.

Keywords

stressantidepressanthippocampusserotonintianeptineimipraminedesipraminetyrosine hydroxylase
Type
Research Article
Information
European Psychiatry , Volume 8 , Issue S2: Neuroendocrinological aspects of depression 28 June 1992, Nice, France , 1993 , pp. 41s - 48s
Copyright
Copyright © Elsevier, Paris 1993

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References

Angulo, JADavis, LBurkhart, BChristoph, G (1986) Reduction of striatal dopaminergic neurotransmission elevates striatal proenkephalin mRNA.Eur J Pharmacol 130,341–343CrossRefGoogle ScholarPubMed
Angulo, JAPrintz, DLedoux, MMcEwen, BS (1991) Isolation stress increases tyrosine hydroxylase mRNA in the locus coeruleus and midbrain and decreases proenkephalin mRNA in the striatum and nucleus accumbens. Mol Brain Res 11,301–308CrossRefGoogle ScholarPubMed
Angulo, J (1992) Involvement of dopamine Dl and D2 receptors in the regulation of proenkephalin mRNA abundance in the striatum and accumbens of the rat brain. J Neurochem 58, 1104–1109CrossRefGoogle Scholar
Anisman, HZacharko, R (1982) Depression: the predisposing influence of stress. Behav Brain Sci 5, 89–137CrossRefGoogle Scholar
Anisman, HIrwin, JBowers, WAhluwalia, PZacharko, M (1987) Variations of norepinephrine concentrations following chronic stressor application. Phann Biochem Behav 26, 653–659CrossRefGoogle ScholarPubMed
Bertorelli, RAmoroso, DGirotti, PConsolo, S (1992) Effect of tianeptine on the central cholinergic system: involvement of serotonin. Naunyn-Schmiedeberg's Arch Pharmacol 345, 276–281CrossRefGoogle Scholar
Bode-Greuel, KKlisch, JHorvath, EGlaser, TTraber, J (1990) Effects of 5-hydroxytryptamine lA-receptor agonists on hippocampal damage after transient forebrain ischemia in the Mongolian gerbil. Stroke 21, 164–166Google Scholar
Brown, RCarlson, BLjunggren, BSiesjo, BSnider, S (1974) Effect of ischemia on monoamine metabolism in the brain. Acta Physiol Scand 90, 789–791CrossRefGoogle Scholar
Chao, HMcEwen, BS (1990) Glucocorticoid regulation of preproenkaphlin messenger ribonucleic acid in the rat striatum. Endocrinology 126, 3124–3130CrossRefGoogle ScholarPubMed
Chao, HMcEwen, BS (1991) Glucocorticoid regulation of neuropeptide mRNAs in the rat striatum. Mol Brain Res 9, 307–311CrossRefGoogle ScholarPubMed
Chrousos, GGold, P (1992) The concepts of stress and stress system disorders. J Am Med Assn 267,1244–1252CrossRefGoogle ScholarPubMed
Day, R (1981) Life events and schizophrenia: the “triggering” hypothesis. Acta Psychiatr Scand 64,97–122CrossRefGoogle ScholarPubMed
Fattaccini, CBolonos-Jimenez, HGozlan, HHamon, M (1990) Tianeptine stimulates uptake of 5-hydroxytryptamine in vivo in the rat brain. Neuropharmacology 29, 1–8CrossRefGoogle ScholarPubMed
Fujikura, HKato, HNakano, SKogure, K (1989) A serotonin S2 antagonists, naftidrofuryl, exhibited a protective effect on ischemic neuronal damage in the gerbil. Brain Res 494, 387–390CrossRefGoogle ScholarPubMed
Gannon, MMcEwen, BS (1990) Calmodulin involvement in stress and corticosterone-induced down-regulation of cyclic AMP-generating systems in brain. J Neurochem 55, 276–284CrossRefGoogle ScholarPubMed
Gilad, GGilad, VWyatt, RTizabi, Y (1990) Regionselective stress-induced increase of glutamate uptake and release in rat forebrain. Brain Res 525, 335–338CrossRefGoogle Scholar
Gold, PGoodwin, FChrousos, G (1988a) Clinical and biochemical manifestations of depression. N Engl J Med 329, 348–353CrossRefGoogle Scholar
Gold, PGoodwin, FChrousos, G (1988b) Clinical and biochemical manifestations of depression. New Engl J Med 319, 413-20CrossRefGoogle Scholar
Invernizzi, RPozzi, LGarattini, SSamanin, R (1992) Tianeptine increases the extracellular concentrations of dopamine in the nucleus accumbens by a serotoninindependent mechanism. Neuropharmacology 31, 221–227CrossRefGoogle ScholarPubMed
Kennet, GDickinson, SCurzon, G (1985) Enhancement of some 5-HT dependent behavioral responses following repeated immobilization in rats. Brain Res 330, 253–263CrossRefGoogle Scholar
Kerr, SCampbell, LApplegate, MBrodish, ALandfield, P (1991) Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J Neurosci 1, 1316–1324CrossRefGoogle Scholar
Langer, SZRaisman, RBriley, M (1981) High-affinity 3H DMI binding is associated with noradrenaline uptake in the periphery and the central nervous system. Eur J Pharmacol 72, 423–424CrossRefGoogle ScholarPubMed
Leviel, VFayada, CGiubert, BChaminade, MMachek, GMallet, JBiguet, N (1990) Short- and long-term alterations of gene expression in limbic structures by repeated electroconvulsive-induced seizures. J Neurochem 54, 899–904CrossRefGoogle Scholar
Louilot, AMocaer, ESimon, HLe Moal, M (1990) Difference in the effects of the antidepressant tianeptine on dopaminergic metabolism in the prefrontal cortex and the nucleus accumbens of the rat. A voltammetric study. Life Sci 47, 1083–1089CrossRefGoogle Scholar
McEwen, BSAngulo, JCameron, HChao, HDaniels, DGannon, MGould, EMendelson, SSakai, RSpencer, RWool ley, C (1992) Paradoxical effects of adrenal steroids on the brain: protection versus degeneration. Biol Psychiatr 31, 177–199CrossRefGoogle ScholarPubMed
McEwen, BSGould, E (1990) Adrenal steroid influences on the survival of the hippocampal neurons. Biochem Pharmacol 40, 2393–2402CrossRefGoogle ScholarPubMed
Mennini, TMocaer, EGarratini, S (1987) Tianeptine, a selective enhancer of serotonin uptake in rat brain. Nauyn-Schmiedenhurg Arch Pharmacol 336, 478–482Google ScholarPubMed
Mennini, TMiari, A (1991) Modulation of 3H glutamate binding by serotonin in rat hippocampus: an autoradiographic study. Life Sci 49, 283–292CrossRefGoogle Scholar
de Montigny, CWeiss, MOuellette, J (1987) Reduced excitatory effect of kainic acid on rat CA3 hippocampal pyramidal neurons following destruction of the mossy projection with colchicine. Exp Brain Res 65, 605–613CrossRefGoogle ScholarPubMed
de Montigny, CPineyro, GChaput, YBlier, P (1992) Electrophysiological studies on the effect of longterm 5HT reuptake inhibition on the function of 5HT neurons. Clin Neuropharmacol 15 (suppl 1 Pt A), 440-441Google Scholar
Murua, VMolina, V (1992) Effect of chronic variable stress and antidepressant drugs on behavioral inactivity during an uncontrollable stress: interaction between both treatments. Behav Neurol Biol 57, 87–89CrossRefGoogle ScholarPubMed
Nadler, JCuthbertson, G (1980) Kainic acid neurotoxicity toward hippocampal formation: dependence on specific excitatory pathways. Brain Res 195, 47–56CrossRefGoogle ScholarPubMed
Nankai, MYamada, SToru, M (1991) Down-regulation of serotonin uptake sites in rat brain induced by concomittant chronic administration of desipramineti and repeated stress. Jap J Psychiatr Neurol 45, 1–106Google Scholar
Nedergaard, SEngber, LFlatman, J (1987) The modulation of excitatory amino acid responses by serotonin in the cat neocortex in vitro. Cell Mol Neurol 7, 367CrossRefGoogle ScholarPubMed
Nisenbaum, LZigmond, MSved, AAbercrombie, E (1991) Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel stressor. J Neurosci 11, 1478–1484CrossRefGoogle ScholarPubMed
Ohi, KMikuni, MTakahashi, K (1989) Stress adaptation and hypersensitivity in 5-HT neuronal systems after repeated foot shock. Pharmacol Biochem Behav 34, 603–608CrossRefGoogle ScholarPubMed
Peroutka, S Snyder|S (1980) Long-term antidepressant treatment decreases spiroperidol-labeled serotonin receptor binding. Science 210, 88–90CrossRefGoogle ScholarPubMed
Richard, FBiguet, NLabatut, RRollet, DMallet, JBuda, M (1988) Modulation of tyrosine hydroxylase gene expression in rat brain ADN adrenals by exposure to cold. J Neurosci Res 20, 32–37CrossRefGoogle Scholar
Richter-Levin, GSegal, M (1988) Serotonin releasers modulate reactivity of the rat hippocampus to afferent stimulation. 94, 173–176Google ScholarPubMed
Romano, GShivers, BHarlan, RHowells, RPfaff, D (1987) Haloperidol increases proenkephalin mRNA levels in the caudate-putamen of the rat: a quantitative study at the cellular level using in situ hybridization. Mol Brain Res 2, 33–41CrossRefGoogle Scholar
Sakaguchi, TNakamura, S (1990) Duration-dependent effects of repeated restraint stress on cortical projections of locus coeruleus neurons. Neurosci Lett 118, 193–196CrossRefGoogle ScholarPubMed
Schaasfoort, EDeBrin, LKorf, J (1988) Mild stress stimulates rat hippocampal glucose utilization transiently via NMDA receptors, as assessed by lactography. Brain Res 575, 58–63CrossRefGoogle Scholar
Segal, DKnapp, SKucsenski, RMandell, A (1973) The effects of environmental isolation on behavioral and regional rat brain tyrosine hydroxylase and tryptophan hydroxylase activities.Behav Biol 8, 47–53CrossRefGoogle ScholarPubMed
Sloviter, R (1983) “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscope studies. Brain Res Bull 10, 675–697CrossRefGoogle Scholar
Sloviter, R (1989) Calcium-binding protein (Calbindin- D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippoeampal neurons to seizure activity. J Comp Neural 280, 183–196CrossRefGoogle Scholar
Stone, E (1983) Problems with current catecholamine hypotheses of antidepressant agents: speculations leading to a new hypothesis. Behav Brain Sci 6, 535–577CrossRefGoogle Scholar
Stone, EMcEwen, BSHerrera, A, Carr, K (1987) Regulation of alpha and beta components of noradrenergic cyclic AMP response in cortical slices. Eur J Pharmacol 141,347–356CrossRefGoogle Scholar
Tang, FCosta, ESchwartz, J (1983) Increase of proenkephalin mRNA and enkephalin content of rat striatum after daily injection of haloperidol for 2-3 weeks. Proc Natl Acad Sci USA 80, 3841–3844CrossRefGoogle Scholar
Tsuda, ATanaka, M (1985) Differential changes in noradrenaline turnover in specific regions of rat brain produced by controllable and uncontrollable shocks. Behav Neurosci 99, 802–817CrossRefGoogle ScholarPubMed
Uno, HTarara, RElse, JSuleman, MSapolsky, R (1989) Hippoeampal damage associated with prolonged and fatal stress in primates. J Neurosci 9, 1705CrossRefGoogle Scholar
Uno, HFlugge, GThieme, CJohren, CFuchs, E (1991) Degeneration of the hippoeampal pyramidal neurons in the socially stressed tree shrew. Abstr Sac Neurosci 17,52.20Google Scholar
Watanabe, YGould, EMcEwen, BS(1992a) Stress induces atrophy of apical dendrites of hippoeampal CA3 pyramidal neurons. Brain Res 588, 341–345CrossRefGoogle Scholar
Watanabe, YGould, ECameron, HADaniels, DCMcEwen, BS (1992b) Phenytoin prevents stress- and corticosterone- induced atrophy of CA3 pyramidal neurons. Hippocampus 2, 431–436CrossRefGoogle Scholar
Watanabe, YGould, EDaniels, DCCameron, HAMcEwen, BS (1992c) Tianeptine attenuates stressinduced morphological change in the hippocampus. Eur J Pharmacol 222, 157–162CrossRefGoogle Scholar
Watanabe, YMcEwen, BSMendelson, S (1993) Stress and antidepressant actions on hippoeampal and cortical 5HT1A and 5HT2 receptors and transport sites for serotonin. Brain Res 615, 87–94CrossRefGoogle Scholar
Weiss, JGoodman, PLosito, BCorrigan, SCharry, JBailey, W (1981) Behavioral depression produced by an uncontrollable stressor: relationship to norepinephrine, dopamine, and serotonin levels in various regions of rat brain. Brain Res Rev 3, 167–205CrossRefGoogle Scholar
Whitton, PSarna, GO'Connell, MCurzon, G (1991) The effect of the novel antidepressant tianeptine on the concentration of 5-hydroxytryptamine in rat hippoeampal dialysates in vivo. Psychopharmacol 104, 81–85CrossRefGoogle Scholar
Woolley, CGould, EMcEwen, BS (1990) Exposures to excess glucocorticoids alters dendritic morphology of adult pyramidal neurons. Brain Res 531, 225–231CrossRefGoogle Scholar
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